Identification of estrogen-responsive proteins in MCF-7 human breast cancer cells using label-free quantitative proteomics

Proteomics

Volumn 8, Issue 10, 2008, Pages 1987-2005

  Zhu, Zheying ^a   Boobis, Alan R ^a   Edwards, Robert J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Differential protein expression; Estrogen; GeLC MS; Label free proteomics

Indexed keywords

ESTROGEN;

ARTICLE; BREAST CANCER; CANCER CELL; CELL LYSATE; CELL PROLIFERATION; DOWN REGULATION; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MOLECULAR WEIGHT; PHYSICAL CHEMISTRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; REPRODUCIBILITY; UPREGULATION;

CELL LINE, TUMOR; DOWN-REGULATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESTRADIOL; ESTROGENS; HUMANS; MASS SPECTROMETRY; PROTEINS; PROTEOMICS; UP-REGULATION;

EID: 44649122799     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200700901     Document Type: Article

References (76)

1. Thomas, T., Gallo, M. A., Thomas, T. J., Estrogen receptors as targets for drug development for breast cancer, osteoporosis and cardiovascular diseases. Curr. Cancer Drug Targets 2004, 4, 483-499.
2. Lorenzo, J., A new hypothesis for how sex steroid hormones regulate bone mass. J. Clin. Invest. 2003, 111, 1641-1643.
3. Pratt, W. B., Toft, D. O., Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev. 1997, 18, 306-360.
4. Acconcia, F., Kumar, R., Signaling regulation of genomic and nongenomic functions of estrogen receptors. Cancer Lett. 2006, 238, 1-14.
5. Bjornstrom, L., Sjoberg, M., Mechanisms of estrogen receptor signaling: Convergence of genomic and nongenomic actions on target genes. Mol. Endocrinol. 2005, 19, 833-842.
6. Morley, P., Whitfield, J. F., Vanderhyden, B. C., Tsang, B. K. et al., A new, nongenomic estrogen action: The rapid release of intracellular calcium. Endocrinology 1992, 131, 1305-1312.
7. Naciff, J. M., Jump, M. L., Torontali, S. M., Carr, G. J. et al., Gene expression profile induced by 17alpha-ethynyl estradiol, bisphenol A, and genistein in the developing female reproductive system of the rat. Toxicol. Sci. 2002, 68, 184-199.
8. Wang, D. Y., McKague, B., Liss, S. N., Edwards, E. A., Gene expression profiles for detecting and distinguishing potential endocrine-disrupting compounds in environmental samples. Environ. Sci. Technol. 2004, 38, 6396-6406.
9. Buterin, T., Koch, C., Naegeli, H., Convergent transcriptional profiles induced by endogenous estrogen and distinct xenoestrogens in breast cancer cells. Carcinogenesis 2006, 27, 1567-1578.
10. Hong, E. J., Park, S. H., Choi, K. C., Leung, P. C. et al., Identification of estrogen-regulated genes by microarray analysis of the uterus of immature rats exposed to endocrine disrupting chemicals. Reprod. Biol. Endocrinol. 2006, 4, 49-60.
11. Malorni, L., Cacace, G., Cuccurullo, M., Pocsfalvi, G. et al., Proteomic analysis of MCF-7 breast cancer cell line exposed to mitogenic concentration of 17beta-estradiol. Proteomics 2006, 6, 5973-5982.
12. Chen, X., Cushman, S. W., Pannell, L. K., Hess, S., Quantitative proteomic analysis of the secretory proteins from rat adipose cells using a 2D liquid chromatography-MS/MS approach. J. Proteome Res. 2005, 4, 570-577.
13. Asara, J. M., Zhang, X., Zheng, B., Christofk, H. H. et al., In-Gel Stable-Isotope Labeling (ISIL): A strategy for mass spectrometry-based relative quantification. J. Proteome Res. 2006, 5, 155-163.
14. Fang, R., Elias, D. A., Monroe, M. E., Shen, Y. et al., Differential label-free quantitative proteomic analysis of Shewanella oneidensis cultured under aerobic and suboxic conditions by accurate mass and time tag approach. Mol. Cell. Proteomics 2006, 5, 714-725.
15. Ono, M., Shitashige, M., Honda, K., Isobe, T. et al., Label-free quantitative proteomics using large peptide data sets generated by nanoflow liquid chromatography and mass spectrometry. Mol. Cell. Proteomics 2006, 5, 1338-1347.
16. Cutillas, P. R., Vanhaesebroeck, B., Quantitative profile of five murine core proteomes using label-free functional proteomics. Mol. Cell. Proteomics 2007, 6, 1560-1573.
17. Old, W. M., Meyer-Arendt, K., Veline-Wolf, L., Pierce, K. G. et al., Comparison of label-free methods for quantifying human proteins by shotgun proteomics. Mol. Cell. Proteomics 2005, 4, 1487-1502.
18. Le, B. T., Goh, T., Stewart, I. I., Salter, A. M. et al., Differential analysis of membrane proteins in mouse fore- and hindbrain using a label-free approach. J. Proteome Res. 2006, 5, 2701-2710.
19. Nicholas, B., Skipp, P., Mould, R., Rennard, S. et al., Shotgun proteomic analysis of human-induced sputum. Proteomics 2006, 6, 4390-4401.
20. Rezaul, K., Wu, L., Mayya, V., Hwang, S. I. et al., A systematic characterization of mitochondrial proteome from human T leukemia cells. Mol. Cell. Proteomics 2005, 4, 169-181.
21. Hansen, M. B., Nielsen, S. E., Berg, K., Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Methods 1989, 119, 203-210.
22. Watson, K., Edwards, R. J., Shaunak, S., Parmelee, D. C. et al., Extra-nuclear location of histones in activated human peripheral blood lymphocytes and cultured T-cells. Biochem. Pharmacol. 1995, 50, 299-309.
23. Edwards, R. J., Targeting antipeptide antibodies toward cytochrome P450 enzymes. Methods Mol. Biol. 2006, 320, 173-182.
24. Albig, W., Runge, D. M., Kratzmeier, M., Doenecke, D., Heterologous expression of human H1 histones in yeast. FEBS Lett. 1998, 435, 245-250.
25. Ogawa, S., Oishi, H., Mezaki, Y., Kouzu-Fujita, M. et al., Repressive domain of unliganded human estrogen receptor alpha associates with Hsc70. Genes Cells 2005, 10, 1095-1102.
26. Ruden, D. M., Xiao, L., Garfinkel, M. D., Lu, X., Hsp90 and environmental impacts on epigenetic states: A model for the trans-generational effects of diethylstibesterol on uterine development and cancer. Hum. Mol. Genet. 2005, 14, R149-R155.
27. Pick, E., Kluger, Y., Giltnane, J. M., Moeder, C. et al., High HSP90 expression is associated with decreased survival in breast cancer. Cancer Res. 2007, 67, 2932-2937.
28. Levin, E. R., Integration of the extranuclear and nuclear actions of estrogen. Mol. Endocrinol. 2005, 19, 1951-1959.
29. Song, R. X., Santen, R. J., Membrane initiated estrogen signaling in breast cancer. Biol. Reprod. 2006, 75, 9-16.
30. Azuma, K., Horie, K., Inoue, S., Ouchi, Y. et al., Analysis of estrogen receptor alpha signaling complex at the plasma membrane. FEBS Lett. 2004, 577, 339-344.
31. Li, X., Qin, C., Burghardt, R., Safe, S., Hormonal regulation of lactate dehydrogenase-A through activation of protein kinase C pathways in MCF-7 breast cancer cells. Biochem. Biophys. Res. Commun. 2004, 320, 625-634.
32. Kumar, P., Mark, P. J., Ward, B. K., Minchin, R. F. et al., Estradiol-regulated expression of the immunophilins cyclophilin 40 and FKBP52 in MCF-7 breast cancer cells. Biochem. Biophys. Res. Commun. 2001, 284, 219-225.
33. Ward, B. K., Mark, P. J., Ingram, D. M., Minchin, R. F. et al., Expression of the estrogen receptor-associated immunophilins, cyclophilin 40 and FKBP52, in breast cancer. Breast Cancer Res. Treat. 1999, 58, 267-280.
34. Moggs, J. G., Tinwell, H., Spurway, T., Chang, H. S. et al., Phenotypic anchoring of gene expression changes during estrogen-induced uterine growth. Environ. Health Perspect. 2004, 112, 1589-1606.
35. Jayakumar, A., Tai, M. H., Huang, W. Y., al-Feel, W. et al., Human fatty acid synthase: Properties and molecular cloning. Proc. Natl. Acad. Sci. USA 1995, 92, 8695-8699.
36. Kuhajda, F. P., Fatty-acid synthase and human cancer: New perspectives on its role in tumor biology. Nutrition 2000, 16, 202-208.
37. Lupu, R., Menendez, J. A., Targeting fatty acid synthase in breast and endometrial cancer: An alternative to selective estrogen receptor modulators? Endocrinology 2006, 147, 4056-4066.
38. Shoulars, K., Brown, T., Alejandro, M. A., Crowley, J. et al., Identification of nuclear type II [(3)H]estradiol binding sites as histone H4. Biochem. Biophys. Res. Commun. 2002, 296, 1083-1090.
39. Shoulars, K., Rodrigues, M. A., Crowley, J. R., Turk, J. et al., Nuclear type II [3H]estradiol binding sites: A histone H3-H4 complex. J. Steroid Biochem. Mol. Biol. 2005, 96, 19-30.
40. Markaverich, B. M., Roberts, R. R., Alejandro, M., Clark, J. H., The effect of low dose continuous exposure to estradiol on the estrogen receptor (type I) and nuclear type II sites. Endocrinology 1984, 114, 814-820.
41. Galande, S., Kohwi-Shigematsu, T., Poly(ADP-ribose) polymerase and Ku autoantigen form a complex and synergistically bind to matrix attachment sequences. J. Biol. Chem. 1999, 274, 20521-20528.
42. Takahagi, M., Tatsumi, K., Aggregative organization enhances the DNA end-joining process that is mediated by DNA-dependent protein kinase. FEBS J. 2006, 273, 3063-3075.
43. Arnold, S. F., Obourn, J. D., Yudt, M. R., Carter, T. H. et al., In vivo and in vitro phosphorylation of the human estrogen receptor. J. Steroid Biochem. Mol. Biol. 1995, 52, 159-171.
44. Likhite, V. S., Stossi, F., Kim, K., Katzenellenbogen, B. S. et al., Kinase-specific phosphorylation of the estrogen receptor changes receptor interactions with ligand, deoxyribonucleic acid, and coregulators associated with alterations in estrogen and tamoxifen activity. Mol. Endocrinol. 2006, 20, 3120-3132.
45. Jaskulski, D., deRiel, J. K., Mercer, W. E., Calabretta, B. et al., Inhibition of cellular proliferation by antisense oligodeoxynucleotides to PCNA cyclin. Science 1988, 240, 1544-1546.
46. Terry, G., Ho, L., Londesborough, P., Duggan, C. et al., The expression of FHIT, PCNA and EGFR in benign and malignant breast lesions. Br. J. Cancer 2007, 96, 110-117.
47. Duncan, R., Bazar, L., Michelotti, G., Tomonaga, T. et al., A sequence-specific, single-strand binding protein activates the far upstream element of c-myc and defines a new DNA-binding motif. Genes Dev. 1994, 8, 465-480.
48. He, L., Weber, A., Levens, D., Nuclear targeting determinants of the far upstream element binding protein, a c-myc transcription factor. Nucleic Acids Res. 2000, 28, 4558-4565.
49. Liu, J., Kouzine, F., Nie, Z., Chung, H. J. et al., The FUSE/FBP/FIR/TFIIH system is a molecular machine programming a pulse of c-myc expression. EMBO J. 2006, 25, 2119-2130.
50. Majid, S. M., Liss, A. S., You, M., Bose, H. R., The suppression of SH3BGRL is important for v-Rel-mediated transformation. Oncogene 2006, 25, 756-768.
51. Delage-Mourroux, R., Martini, P. G., Choi, I., Kraichely, D. M. et al., Analysis of estrogen receptor interaction with a repressor of estrogen receptor activity (REA) and the regulation of estrogen receptor transcriptional activity by REA. J. Biol. Chem. 2000, 275, 35848-35856.
52. Guitard, E., Parker, F., Millon, R., Abecassis, J. et al., G3BP is overexpressed in human tumors and promotes S phase entry. Cancer Lett. 2001, 162, 213-221.
53. Dresios, J., Panopoulos, P., Synetos, D., Eukaryotic ribosomal proteins lacking a eubacterial counterpart: Important players in ribosomal function. Mol. Microbiol. 2006, 59, 1651-1663.
54. Chiao, P. J., Shin, D. M., Sacks, P. G., Hong, W. K. et al., Elevated expression of the ribosomal protein S2 gene in human tumors. Mol. Carcinog. 1992, 5, 219-231.
55. Shin, D. M., Chiao, P. J., Sacks, P. G., Shin, H. J. et al., Activation of ribosomal protein S2 gene expression in a hamster model of chemically induced oral carcinogenesis. Carcinogenesis 1993, 14, 163-166.
56. Nagai, M. A., Ros, N., Bessa, S. A., Mourao, N. M. et al., Differentially expressed genes and estrogen receptor status in breast cancer. Int. J. Oncol. 2003, 23, 1425-1430.
57. Tasheva, E. S., Ariyasu, T., Matsuo, Y., Drexler, H. G. et al., Possible new genetic marker for human lymphoid leukemias as detected by ribosomal protein S14 cDNA. Leukemia 1993, 7, 318-322.
58. Karan, D., Kelly, D. L., Rizzino, A., Lin, M. F. et al., Expression profile of differentially-regulated genes during progression of androgen-independent growth in human prostate cancer cells. Carcinogenesis 2002, 23, 967-975.
59. Lexander, H., Palmberg, C., Auer, G., Hellstrom, M. et al., Proteomic analysis of protein expression in prostate cancer. Anal. Quant. Cytol. Histol. 2005, 27, 263-272.
60. Chester, K. A., Robson, L., Begent, R. H., Talbot, I. C. et al., Identification of a human ribosomal protein mRNA with increased expression in colorectal tumours. Biochim. Biophys. Acta 1989, 1009, 297-300.
61. Kim, T. S., Jang, C. Y., Kim, H. D., Lee, J. Y. et al., Interaction of Hsp90 with ribosomal proteins protects from ubiquitination and proteasome-dependent degradation. Mol. Biol. Cell 2006, 17, 824-833.
62. Al-Maghrebi, M., Anim, J. T., Olalu, A. A., Up-regulation of eukaryotic elongation factor-1 subunits in breast carcinoma. Anticancer Res. 2005, 25, 2573-2577.
63. Chen, L., Madura, K., Increased proteasome activity, ubiquitin- conjugating enzymes, and eEF1A translation factor detected in breast cancer tissue. Cancer Res. 2005, 65, 5599-5606.
64. Tomlinson, V. A., Newbery, H. J., Wray, N. R., Jackson, J. et al., Translation elongation factor eEF1A2 is a potential oncoprotein that is overexpressed in two-thirds of breast tumours. BMC Cancer 2005, 5, 113.
65. Eufemi, M., Coppari, S., Altieri, F., Grillo, C. et al., ERp57 is present in STAT3-DNA complexes. Biochem. Biophys. Res. Commun. 2004, 323, 1306-1312.
66. Yano, M., Terada, K., Mori, M., Mitochondrial import receptors Tom20 and Tom22 have chaperone-like activity. J. Biol. Chem. 2004, 279, 10808-10813.
67. Gruvberger, S., Ringner, M., Chen, Y., Panavally, S. et al., Estrogen receptor status in breast cancer is associated with remarkably distinct gene expression patterns. Cancer Res. 2001, 61, 5979-5984.
68. Bonnet, S., Archer, S. L., Ialunis-Turner, J., Haromy, A. et al., A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell 2007, 11, 37-51.
69. Sharma, M., Henderson, B. R., IQ-domain GTPase-activating protein 1 regulates beta-catenin at membrane ruffles and its role in macropinocytosis of N-cadherin and adenomatous polyposis coli. J. Biol. Chem. 2007, 282, 8545-8556.
70. Le, C. C., Schlaepfer, D., Ferrari, A., Klingauf, M. et al., IQGAP1 stimulates actin assembly through the N-WASP-Arp2/3 pathway. J. Biol. Chem. 2007, 282, 426-435.
71. Frasor, J., Danes, J. M., Komm, B., Chang, K. C. et al., Profiling of estrogen up- and down-regulated gene expression in human breast cancer cells: Insights into gene networks and pathways underlying estrogenic control of proliferation and cell phenotype. Endocrinology 2003, 144, 4562-4574.
72. Nabeshima, K., Shimao, Y., Inoue, T., Koono, M., Immunohistochemical analysis of IQGAP1 expression in human colorectal carcinomas: Its overexpression in carcinomas and association with invasion fronts. Cancer Lett. 2002, 176, 101-109.
73. Feng, Y., Walsh, C. A., The many faces of filamin: A versatile molecular scaffold for cell motility and signalling. Nat. Cell Biol. 2004, 6, 1034-1038.
74. Kammerer, S., Roth, R. B., Hoyal, C. R., Reneland, R. et al., Association of the NuMA region on chromosome 11q13 with breast cancer susceptibility. Proc. Natl. Acad. Sci. USA 2005, 102, 2004-2009.
75. Zimmer, D. B., Cornwall, E. H., Landar, A., Song, W., The S100 protein family: History, function, and expression. Brain Res. Bull. 1995, 37, 417-429.
76. Memon, A. A., Sorensen, B. S., Meldgaard, P., Fokdal, L. et al., Down-regulation of S100C is associated with bladder cancer progression and poor survival. Clin. Cancer Res. 2005, 11, 606-611.